Post-fire structural and compositional habitat resilience in pine plantations woodland types

doi:10.21203/rs.3.rs-1723531/v1

Fire plays a key role in structuring biotic communities around the world. In fire-prone regions, many plant species have acquired adaptive traits (seeders and resprouters) that help them to survive, reproduce, and persist after fire disturbances. Seeder and resprouter species have different short-term responses to fire. Obligate seeders have faster growth rates, greater allocation to reproduction, shorter life cycles, and lower shade tolerance than resprouters. A few years after fire, obligate seeders are expected to be more abundant than resprouter species within post-fire plant communities. We examined this hypothesis in burnt pine plantations located along the African rim of the Western Mediterranean Basin. In this region, pine plantation is the commonest forestry practice, and such woodlands have undergone frequent fires during the last decades. Here, we describe habitat structure and plant species composition in burnt and unburnt plots located in four independent burnt sites. Burnt and unburnt plots were structurally different, with the shrub and grass covers expanding after fire. In terms of functional plant composition, seeders were more abundant than resprouters in burnt pine plantations. The stronger short-term resilience of obligate seeders compared to resprouters was found to be related to the faster capacity of obligate seeders to respond to fire. Contrast in fire response between the two functional plant groups needs to be addressed in conservation planning to ensure the preservation of biodiversity in a future scenario of change in fire regime.

Fire

Pine plantations

Seeder

Resprouter

Structure vegetation

Resilience

Basin Mediterranean

Fire, a recurrent disturbance affecting many terrestrial regions, defines the structure of the landscape and the composition of biotic communities (Bond and Van Wilgen 1996; Pausas and Keeley 2009; Keeley et al. 2012). For many biomes, fire is considered an essential process beneficial to ecosystem functioning (Bond and van Wilgen 1996; Bond et al. 2005). In fire-prone ecosystems, natural fire regimes are conducive to the resilience of these communities, i.e. species composition returns to its pre-fire profile (Keeley and Pausas 2019). However, forest resilience is currently undergoing widespread disruption due to fire-regime shifts (e.g. changes in fire frequency, intensity and extension) caused a combination of global warming (McKenzie et al. 2004) and socioeconomic changes (e.g. land abandonment and fuel increase (Pausas et al. 2012; Pausas and Fernández-Muñoz 2012)). Understanding how vegetation responds to fire is therefore critical for predicting the properties and species composition of many ecosystems (Smith et al. 1997; Lavorel and Cramer 1999).

The response of plant species to fire is driven by a combination of species-specific resistance and resilience traits (Clarke et al. 2013; Lawes et al. 2016). Resistance traits are based on structures such as thick bark and tall crown that protect plant tissues from deadly temperatures, whereas resilience traits such as resprouting ability from unburnt tissues allow individuals to recover after fire (Lawes et al. 2016). In Mediterranean ecosystems, wildfires are natural disturbances influencing vegetation dynamics (Trabaud 1981), acting as an evolutionary pressure that shapes plant traits (Keeley et al. 2012). Based on these traits, species can be divided into seeders, resprouters, and facultative seeders (Pausas 1999b; Verdú 2000), which have different seedling density and survival following wildfires (Benwell 1998). Seeder species may die during fire, but their populations recover by seed germination (Keeley et al. 2012), this depending heavily on adequate soil moisture and temperature (Bewley et al. 2013; Chamorro et al. 2017). Resprouter species recover in situ from fire by resprouting from buds located in aerial, basal or underground organs that are more or less protected by leaves, bark, or soil (Klimešová and Klimeš 2007; Clarke et al. 2013). Intermediate between these two extremes are facultative seeders species, which have the ability to couple both resprouting and seeding in their mode of postfire recovery (Keeley 1986).

Previous studies have investigated differences in growth dynamics of various post-fire regeneration strategies (Pausas and Keeley 2014; Vilagrosa et al. 2014; Parra and Moreno 2017; Cooper et al. 2018). Some studies have found that these regeneration strategies vary regarding allocation of resources (Hansen et al. 1991; Bell et al. 1996). Kruger et al. (1997) discovered that seedlings from seeders develop more quickly than those from resprouters, since seeders devote more resources to stems while resprouters allocate more resources to underground organs. Additionally, it has been found that seeders have higher drought tolerance than do resprouters and are thus more abundant in xeric areas (Keeley 1986; Pausas et al. 2004; Correia and Catarino 1996; Saura 2005). On the other hand, some studies have found that seedlings have just a few months of good conditions to establish a root system extensive enough to reach deep water sources before summer drought (Hastings et al. 1989; Castell et al. 1994; Fleck et al. 1995). As a result, seedlings face more significant water restrictions than resprouts and thus undergo substantial mortality during the first year(s) after a fire (Clemente et al. 2005). Furthermore, resprouting plants do not necessarily cede the space occupied to competitors after fire, unlike seeders (Ojeda et al. 2005). Thus, notwithstanding the seeming advantage of the resprouting life history in terms of fitness, fire-prone floras often contain a greater number of seeder species (Wells 1969; Lamont and Markey 1995; Ojeda 1998).

In this study, we examine short-term responses to fire by resprouter and seeder plant species in pine plantations from northwestern Morocco at the Mediterranean basin. In this region, pines have been used for reforestation, especially since the 19th century (Pausas 2015). While these plantations are not naturally fire-adapted forest habitats, they are considered the most efficient means of reforestation after a fire, and are often planted in areas with historically frequent fire-return intervals (Castro 2021).

Here we compare vegetation structure as well as the taxonomic and functional plant composition of burnt and unburnt plots in four pine plantations, which burned in the last 10 years within Tetouan province, Morocco. Given the simplification of the vegetation structure caused by the high and artificial canopy in pine plantations (Chergui et al. 2018b), we expect an increased complexity of the understory and midstory layers following a fire. Most obligate seeders have faster growth rates, greater allocation to reproduction, shorter life cycles, and lower shade tolerance than do resprouters (Verdú 2000; Bell 2001; Bond and Midgley 2001). Accordingly, we hypothesize that a few years after fire, obligate seeders may be more abundant in the post-fire than resprouter species.

Study area

This study was conducted in four forested sites composed by burnt pine plantation in the province of Tetouan (35.589° N; 5.363° W, Fig. 1), on the Tangier Peninsula, forming the Western end of the Rif of northwestern Morocco (Delga et al. 1962). This province covers an area of 2574 km², of which 40% is forest land (Kichou et al. 2003; Ettakifi et al. 2019). The native vegetation is a Mediterranean scrubland, and forest patches (mainly in mountainous areas) are dominated by Cork oak (Quercus suber) (13850 ha), Holm oak (Quercus ilex (1842 ha), Canary Island oak (Quercus canariensis) (1260 ha), and reforested at many sites by conifer plantations (11557 ha) (Ettakifi et al. 2019). Bioclimatically, it occupies the thermo-Mediterranean belt, with two main seasons: a hot and dry season between May and September, and a rainy and cold season from October to April (Elmoulat et al. 2021). The average annual temperature is 22°C, with a range of 35°C-8°C (Ettakifi et al. 2019), and the average annual rainfall reaches 728 mm (Aboulaich et al. 2013). This area is characterized by moderate fire activity during the fire season, which lasts from early June through late September (Chergui et al. 2018a). In the period 2009–2018, 363 fires were registered, and the total surface burnt was approximately 1830 ha, with an average burnt area of 200 hectares per year (Agency for Water and Forests, 2019).

Site selection and vegetation sampling

We selected four pine plantations which burned between 2012 and 2019 and were further managed with salvage logging (i.e. removal of all the burnt wood). The fire history of each site was taken from the http://sysfeu.com (see also Sup Mat Table S1). At each site, six to eight sampling points (3–4 burnt and 3–4 unburnt at each site) were randomly assigned for vegetation sampling. Assuming that the vegetation in the control area remains unchanged and reflects the original pre-fire vegetation composition (Chergui et al. 2018b), unburnt sampling points were selected around each burnt area, usually close to each unburnt pair.

At each sampling point, habitat structure and plant species composition were measured on 6 circular plots (radius 2.5 m) 10 m apart. For each circular plot, we examined three vegetation layers: the overstory, which consisted primarily of trees forming the highest canopy; the midstory, which basically was composed of shrubs; and the understory, which consisted of grasses and other ground covers. Specifically, we measured the extent (percentage of cover) of three vegetation types, namely tree, shrub, and grass, plus the extent of bare ground, death trunks, and litter. The maximum vegetation height (MVH) was also measured in each plot. The percentage of these variables was evaluated visually in each case. The habitat complexity was estimated by calculating the Simpson diversity Index (hereafter Simpson-HAB) based on the percentage of all the vegetation and ground cover types in each plot. We assumed that higher Simpson scores meant greater complexity of the habitat structure.

Plant species composition was determined for each plot by classifying all plants to the species level, as well as estimating the percentage of cover for each species, the latter estimated using a modified Daubenmire (1959) scale (1 = 0–1% cover, 2 = 2–5% cover, 3 = 6–25% cover, 4 = 26–50% cover, 5 = 51–75% cover, 6 = 76–95% cover, 7 = 96–100% cover). Similar to the Simpson index for habitat structure, a species-based Simpson diversity index per plot (hereafter Simpson-SP) was used based on the extent of each plant species. Additionally, all plant species identified were classified according to their plant regenerative ability after fire as a seeder, resprouter, and facultative seeder species, using the information compiled in the BROT database (Paula et al. 2009; Paula and Pausas 2013).

Data analysis

The data for the six circular plots at each sampling point were combined to avoid spatial pseudoreplication. We examined differences between burnt and unburnt pine plantations regarding eight structural variables (Tree canopy cover, Shrub cover, Grass cover, Bare ground cover, Trunk cover, Litter cover, MVH, and Simpson-HAB), two taxonomic ones (Species richness and Simpson-SP), and three functional ones (the number of resprouter, seeder and facultative species).

Generalized Linear Mixed Models (GLMMs) were used to examine the importance of fire condition (i.e. burnt or unburnt ) on the structural, taxonomic, and functional variables, with site as a random effect. The Poisson error distribution was used to analyze variables consisting of count data, and the Gaussian error distribution was used for continuous variables. GLMMs were performed using the lme4 package (Bates et al. 2015) and plots of loess smooth curves with the ggplot2 package (Wickham 2009).

Also, we performed a redundancy analysis (RDA) to identify the association between, on one hand each plant species and functional group, and, on the other, their presence and cover in unburnt and burnt plots. RDA is an extension of multiple regression methods for modelling multivariate response data (Legendre and Legendre, 2012). We calculated the significance of the explained variance in the RDA by performing ANOVA-like permutation tests (9999 permutations), using the RDA function in the vegan package (Oksanen et al. 2018). All the statistical analyses and plots were made with R (R Development Core Team 2020).

We detected significant variation in almost all structural variables between burnt and unburnt sampling points (Table 1; Supplementary Table S1). Tree, bare ground, trunk, and litter covers, as well as MVH and the Simpson index, decreased from unburnt to burnt plots, whereas shrub and grass covers increased with fire.

Table 1

Summary results of generalized mixt model (GLMMs), for the effect of fire on vegetation structural and composition variables. z values are presented for models using the Poisson distribution) and t values are presented for all other variables (Gaussian distribution). ns: not significant test.
Response variable	Fire condition
Response variable	Estimate	z/t value	P
Vegetation structural
Canopy cover	1.8934	17.226	< 0.0001
Shrubs cover	-0.15604	-3.156	0.0016
Grass cover	-0.336455	-93.69	< 0.0001
M.V.H	0.53614	15.78	< 0.0001
Bare ground cover	0.22792	3.965	< 0.0001
Trunk cover	1.26497	16.62	< 0.0001
Litter cover	1.20088	17.97	< 0.0001
Simpson-HAB	0.09454	3.619	0.000296
Vegetation compositional
Species richness	-0.07581	-0.617	ns
Abundance of seeder plants	-1.28533	-38.99	< 0.0001
Abundance of resprouter plants	0.10515	3.32	0.000899
Abundance of facultative seeder plants	-0.81565	-9.327	< 0.0001
Simpson-SP	-0.01841	-0.307	ns

A total of 48 plant species were recorded in burnt and unburnt plots, belonging to 26 taxonomic families (Supplementary Table S2). In both burnt and unburnt points, the midstory is composed mainly of esprouting shrubs such as Arbutus sp., Erica arborea, and obligate seeders such as Cistus sp., especially at burnt points. The GLMMs showed significant functional-group differences with fire, as the abundance of obligate and facultative seeders increased from unburnt to burnt points, whereas resprouter species decreased (Fig. 3).

The RDA confirmed that the functional composition of plant species varied after fire (F = 2.4553, p = 0.009). The first two axes of the RDA explained 69.71% of the total variance. The first axis (43.53% of explained variance; F = 6.739, p = 0.001) was strongly associated with obligate seeders, whereas the second axis (26.18% of explained variance; F = 4.530, p = 0.001), was related to resprouter species (Fig. 4). Notably, most plant species and specifically seeders showed an association with the burnt point, whereas resprouters were related to both burnt and unburnt points.

In our study system, this trend was observed as the plant communities responded to fire at structural, taxonomic and functional levels.

Mediterranean vegetation is fire adapted (i.e. highly resilient), meaning that almost all perennial species can recover after a fire (Pausas and Vallejo 1999; Buhk et al. 2006; Chergui et al. 2018b). By contrast, less diversified systems such as pine plantations are less resilient to natural disturbance than are more complex ecosystems (Drever et al. 2006; Chergui et al. 2018b). Accordingly, pre-and post-fire pine plantations can (taxonomically and structurally) vary (Chergui et al. 2018b). Dense Pinus woodland canopies make pine plantations more susceptible to high-intensity burning compared with open canopies (Keeley et al. 2012). These findings support slow post-fire recovery of pine plantations, particularly throughout dry regions, within the first years after fire (Trabaud 1982; Domínguez et al. 2002; Perula et al. 2003). In addition, inter-specific competition, primarily for water or light, influences the effectiveness of pine re-establishment (Elliott and White 1987; De las Heras et al. 2002). For example, intensive competition with Cistus shrubs during the early stages of succession might drastically retard the development of pine seedlings (Ne'eman 1997). Indeed, we found that burnt plots had a higher percentage of shrubs than did neighboring unburned ones. Several factors could explain this result: first, light transmission is greater beneath low canopies, favoring the establishment of a denser shrub cover (Coll et al. 2011), and fostering plant species richness (Schiller et al. 1997); and second, in areas with low soil moisture such as our Mediterranean study region, shrubs are strong competitors with young seedlings, at least until the latter develop a deep root structure (Plamboeck et al. 2008). In addition, we observed far denser grass cover in burnt vs. unburnt plots. The greater abundance of persistent and annual herbs in burnt plots has been outlined as an opportunistic and transient process facilitated by diminished competitive pressure from woody species that produce shade and compete for nutrients, as well as the sudden availability of nutrients from incinerated organic matter (Trabaud 1982; Calvo et al. 2002, 2003).

The most evident result of our study is that vegetation composition considerably changed in burnt compared to the unburnt plots in pine plantations. This trend was especially visible at the functional level, i.e. the relative abundances of the three regeneration plant types which showed a significant effect of fire. Notably, obligate and facultative seeder species increased from unburnt to burnt points whereas resprouter species decreased. These results support our hypothesis suggesting that over the short term, fire acts as a selective force promoting the obligate-seeder strategy, which would take advantage of the competition-free environmental conditions found after a fire (Schwilk and Ackerly 2001; Pausas et al. 2002). This trend would indicate that seeder species are quite resilient to fire (Parra and Moreno, 2018), supporting a better performance of seeder species in highly disturbed and dry ecosystems (Coca and Pausas 2012) compared to resprouter species.

Obligate seeders significantly proliferate after fire because most have fire-resistant seed banks, and fire can enhance seed germination (Thanos et al. 1992; Arianoutsou and Thanos 1996), generating massive post-fire seedling densities (Ojeda et al. 1996; Lloret 1998). Moreover, seeders have faster growth and higher reproduction rates, shorter life cycles, and stronger shade tolerance, allowing them to be more dominant at the post-fire short term (Pausas et al. 2004; Pausas and Verdú 2005). By contrast, resprouters have slower growth rates than those of obligate seeders (Arnan et al. 2007). Lloret (1998) demonstrated that the recruitment of obligate resprouters occurred only between fires and was connected with the existence of vegetative cover (i.e. Arbutus unedo, Pistacia lentiscus). Throughout this ecological system, when wildfires release resources for establishment, seeders can profit from rapid seedling development as adult resprouters send out new shoots (Verdù 2000). Therefore, when the original community contains a large proportion of obligate seeders, fewer unfilled niches may be available to colonizer species, and the overall community re-establishment becomes stronger (Arnan et al. 2007). In our study system, Cistus monspeliensis and C. crispus are the most common obligate seeders, and they tend to establish abundantly after fire (Franquesa 1995; Lloret et al. 2003). Their seeds are dormant unless disturbed, as by the heat of a fire, friction when moving the soil, or solar heat on the ground of a vegetation gap (Coca and Pausas 2012).

The low rainfall rate and seasonality can also explain the functional response of plant species to fire in our pine plantations. In Mediterranean-type environments, where water availability can be a limited element, a dryness gradient determines regional patterns of vegetation composition (Archibold 1995). Importantly, the proportion of functional groups with post-fire regeneration strategy varies with the water deficit (Pausas 1999a). Seeder species are likely to have characteristics that enable them to survive during drought periods, such as exceedingly small and thick leaves, summer semi-deciduous leaves, or more efficient water use (Paula and Pausas 2006; Pratt et al. 2007). Therefore, when the environment becomes more xeric and arid, resprouting species are frequently replaced by obligate seeding species (Keeley, 1986). As a result, the abundance of resprouters declines and that of obligate seeders augments (Pausas et al. 2004, Lloret et al. 2005). All these factors support the taxonomic and functional response of resprouter and seeder species in our study region.

This study's findings suggest that wildfires affect the habitat structure and the functional composition of plant communities in Moroccan Mediterranean pine plantations, facilitating changes to alternate stable states (Vilà-Cabrera et al. 2008). Although forest communities that develop under more suitable climatic conditions in terms of soil moisture recover quickly, maquis communities, particularly those at lower elevations and drier locations, can take up to 20 years to reestablish their pre-fire structure and composition (Xofis et al. 2021). This slow recovery is caused by the slow rates at which resprouting species reestablish ground cover. On the other hand, obligate seeders, by extending their cover, rapidly dominate the areas. The dry conditions are most likely to blame for the sluggish recovery of these fire-prone communities (Xofis et al. 2021). Based on a projected increase of wildfire recurrence and water stress because of land use and climate changes, some shrub species in the Mediterranean basin would not adapt to these disturbances despite their post-fire regeneration capacity (Vilà-Cabrera et al. 2008). Therefore, there is an urgent need to develop management strategies for increasing Mediterranean-type forests resilience (Pausas 2004).

Conflict of interest: No conficts of interest were identifed.

Acknowledgments We also wish to thank the National Agency for Water and Forests (ANEF) for providing fire information on the Rif. We are grateful to M. Mediani for the kindness and help in the fieldwork. David Nesbitt edited the English style of the text.

Authors contributions MK, BC, SF and XS conceived and designed the research; MK, BC, HZ, YK, AT and SF collected the field data; BC analyzed the data; MK, BC and XS wrote the manuscript.

Funding This study was partially funded by Instituto de Estudios Ceuties (Research grant 2019) and Abdelmalek Essaadi University the Atic Projects (Research grant 2020). This work was also supported by a PhD fellowship from the National Center for Scientific and Technical Research CNRST granted to MK (Excellency research grant-16UAE2020).

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Table 1 Summary results of generalized mixt model (GLMMs), for the effect of fire on vegetation structural and composition variables. z values are presented for models using the Poisson distribution) and t values are presented for all other variables (Gaussian distribution). ns: not significant test.

Response variable	Fire condition
Response variable	Estimate	z/t value	P
Vegetation structural
Canopy cover	1.8934	17.226	< 0.0001
Shrubs cover	-0.15604	-3.156	0.0016
Grass cover	-0.336455	-93.69	< 0.0001
M.V.H	0.53614	15.78	< 0.0001
Bare ground cover	0.22792	3.965	< 0.0001
Trunk cover	1.26497	16.62	< 0.0001
Litter cover	1.20088	17.97	< 0.0001
Simpson-HAB	0.09454	3.619	0.000296
Vegetation compositional
Species richness	-0.07581	-0.617	ns
Abundance of seeder plants	-1.28533	-38.99	< 0.0001
Abundance of resprouter plants	0.10515	3.32	0.000899
Abundance of facultative seeder plants	-0.81565	-9.327	< 0.0001
Simpson-SP	-0.01841	-0.307	ns

No competing interests reported.

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Post-fire structural and compositional habitat resilience in pine plantations woodland types

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Abstract

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Introduction

Materials And Methods

Study area

Site selection and vegetation sampling

Data analysis

Results

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References

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